Full genome sequence of a new polymycovirus infecting Fusarium redolens

Mahillon, Mathieu; Decroës, Alain; Liénard, Charlotte; Bragard, Claude; Legrève, Anne

doi:10.1007/s00705-019-04301-1

Cited by 19 publications

(23 citation statements)

References 22 publications

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“…All known polymycoviruses share four conserved genomic segments, called dsRNA1, dsRNA2, dsRNA3, and dsRNA4, which encode P1 (RNA-dependent RNA polymerase, RdRP), P2 (hypothetical protein with unknown function, containing a transmembrane domain and a zinc-finger motif), P3 (putative methyltransferase, MTR), and P4 (a potential genome-associated protein named proline-alanine-serine-rich protein, PASrp), respectively (Kanhayuwa et al, 2015;Zhai et al, 2016;Jia et al, 2017;Kotta-Loizou and Coutts, 2017;Niu et al, 2018;Mahillon et al, 2019;Nerva et al, 2019; and unpublished sequence data deposited in DDBJ/EMBL/GenBank). Several polymycoviruses have additional one to four genomic segments, among which no significant sequence similarities were found (Zhai et al, 2016;Jia et al, 2017;Kotta-Loizou and Coutts, 2017;Mahillon et al, 2019). Hadakavirus is a novel (+)RNA virus that has a close phylogenetic relationship with polymycoviruses (Sato et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Molecular Characterization of a Novel Polymycovirus From Penicillium janthinellum With a Focus on Its Genome-Associated PASrp

et al. 2020

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The genus Polymycovirus of the family Polymycoviridae accommodates fungal RNA viruses with different genomic segment numbers (four, five, or eight). It is suggested that four members form no true capsids and one forms filamentous virus particles enclosing double-stranded RNA (dsRNA). In both cases, viral dsRNA is associated with a viral protein termed "proline-alanine-serine-rich protein" (PASrp). These forms are assumed to be the infectious entity. However, the detailed molecular characteristics of PASrps remain unclear. Here, we identified a novel five-segmented polymycovirus, Penicillium janthinellum polymycovirus 1 (PjPmV1), and characterized its purified fraction form in detail. The PjPmV1 had five dsRNA segments associated with PASrp. Density gradient ultracentrifugation of the PASrp-associated PjPmV1 dsRNA revealed its uneven structure and a broad fractionation profile distinct from that of typical encapsidated viruses. Moreover, PjPmV1-PASrp interacted in vitro with various nucleic acids in a sequence-non-specific manner. These PjPmV1 features are discussed in view of the diversification of genomic segment numbers of the genus Polymycovirus.

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Section: Introductionmentioning

confidence: 99%

Molecular Characterization of a Novel Polymycovirus From Penicillium janthinellum With a Focus on Its Genome-Associated PASrp

et al. 2020

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“…Six published and four unpublished polymycoviruses with genomic sequences deposited in public databases have been nominated as members of a proposed dsRNA virus taxon, the genus "Polymycovirus" in the family "Polymycoviridae" in the realm Riboviria, according to the taxonomy proposal submitted to the ICTV (ICTV ratified [https://talk.ictvonline.org/files/proposals/ taxonomy_proposals_fungal1/m/fung04/9294]). These 10 candidates were isolated from different fungal species but share four conserved genomic RNA segments, termed dsRNA1, dsRNA2, dsRNA3, and dsRNA4, that putatively encode an RdRP, a protein with unknown function (containing a transmembrane domain and a zinc-finger-like motif), a methyltransferase (MTR), and a proline-alanine-serine-rich protein (PASrp), respectively (15,(17)(18)(19)(20)(21)(22). In addition to the four conserved genomic segments, some polymycoviruses have an additional one to four segments that share no similarity in their sequence to each other and to known protein sequences (17)(18)(19)(20).…”

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Hadaka Virus 1: a Capsidless Eleven-Segmented Positive-Sense Single-Stranded RNA Virus from a Phytopathogenic Fungus, Fusarium oxysporum

Sato

Shamsi

Jamal

et al. 2020

mBio

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The search for viruses infecting fungi, or mycoviruses, has extended our knowledge about the diversity of RNA viruses, as exemplified by the discovery of polymycoviruses, a phylogenetic group of multisegmented RNA viruses with unusual forms. The genomic RNAs of known polymycoviruses, which show a phylogenetic affinity for animal positive-sense single-stranded RNA [(+)RNA] viruses such as caliciviruses, are comprised of four conserved segments with an additional zero to four segments. The double-stranded form of polymycovirus genomic RNA is assumed to be associated with a virally encoded protein (proline-alanine-serine-rich protein [PASrp]) in either of two manners: a capsidless colloidal form or a filamentous encapsidated form. Detailed molecular characterizations of polymycoviruses, however, have been conducted for only a few strains. Here, a novel polymyco-related virus named Hadaka virus 1 (HadV1), from the phytopathogenic fungus Fusarium oxysporum, was characterized. The genomic RNA of HadV1 consisted of an 11-segmented positive-sense RNA with highly conserved terminal nucleotide sequences. HadV1 shared the three conserved segments with known polymycoviruses but lacked the PASrp-encoding segment. Unlike the known polymycoviruses and encapsidated viruses, HadV1 was not pelleted by conventional ultracentrifugation, possibly due to the lack of PASrp. This result implied that HadV1 exists only as a soluble form with naked RNA. Nevertheless, the 11 genomic segments of HadV1 have been stably maintained through host subculturing and conidiation. Taken together, the results of this study revealed a virus with a potential novel virus lifestyle, carrying many genomic segments without typical capsids or PASrp-associated forms. IMPORTANCE Fungi collectively host various RNA viruses. Examples include encapsidated double-stranded RNA (dsRNA) viruses with diverse numbers of genomic segments (from 1 to 12) and capsidless viruses with nonsegmented (+)RNA genomes. Recently, viruses with unusual intermediate features of an infectious entity between encapsidated dsRNA viruses and capsidless (+)RNA viruses were found. They are called polymycoviruses, which typically have four to eight dsRNA genomic segments associated with one of the virus-encoded proteins and are phylogenetically distantly related to animal (+)RNA caliciviruses. Here, we identified a novel virus phylogenetically related to polymycoviruses, from the phytopathogenic fungus Fusarium oxysporum. The virus, termed Hadaka virus 1 (HadV1), has 11 (+)RNA genomic segments, the largest number in known (+)RNA viruses. Nevertheless, HadV1 lacked a typical structural protein of polymycoviruses and was not pelleted by standard ultracentrifugation, implying an unusual capsidless nature of HadV1. This study reveals a potential novel lifestyle of multisegmented RNA viruses.

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“…The majority of characterized mycoviruses of plant-pathogenic fungi have double-stranded RNA (dsRNA) genomes. Mycoviruses with dsRNA genomes have been classified into eight families (the families Totiviridae, Partitiviridae, Chrysoviridae, Amalgaviridae, Curvulaviridae, Reoviridae, Megavirnaviridae, and Polymycoviridae; Several unsigned viruses including AfuPmV-1 have recently been established as a new family Polymycoviridae (Zhai et al, 2016;Jia et al, 2017;Kotta-Loizou and Coutts, 2017b;Niu et al, 2018;Zoll et al, 2018;Mahillon et al, 2019;Sato et al, 2020) (International Committee on Taxonomy of Viruses (ICTV) 1 . Although many mycoviruses do not appear to cause symptoms in their hosts, some affect mycelial growth, sporulation, and pigmentation, while in some botanical pathogenic fungi, mycoviruses have been shown to reduce their virulence in plant hosts (Pearson et al, 2009).…”

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Phenotypic and Molecular Biological Analysis of Polymycovirus AfuPmV-1M From Aspergillus fumigatus: Reduced Fungal Virulence in a Mouse Infection Model

et al. 2020

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The filamentous fungal pathogen Aspergillus fumigatus is one of the most common causal agents of invasive fungal infection in humans; the infection is associated with an alarmingly high mortality rate. In this study, we investigated whether a mycovirus, named AfuPmV-1M, can reduce the virulence of A. fumigatus in a mouse infection model. AfuPmV-1M has high sequence similarity to AfuPmV-1, one of the polymycovirus that is a capsidless four-segment double-stranded RNA (dsRNA) virus, previously isolated from the genome reference strain of A. fumigatus, Af293. However, we found the isolate had an additional fifth dsRNA segment, referred to as open reading frame 5 (ORF5), which has not been reported in AfuPmV-1. We then established isogenic lines of virus-infected and virus-free A. fumigatus strains. Mycovirus infection had apparent influences on fungal phenotypes, with the virus-infected strain producing a reduced mycelial mass and reduced conidial number in comparison with these features of the virus-free strain. Also, resting conidia of the infected strain showed reduced adherence to pulmonary epithelial cells and reduced tolerance to macrophage phagocytosis. In an immunosuppressed mouse infection model, the virus-infected strain showed reduced mortality in comparison with mortality due to the virus-free strain. RNA sequencing and high-performance liquid chromatography (HPLC) analysis showed that the virus suppressed the expression of genes for gliotoxin synthesis and its production at the mycelial stage. Conversely, the virus enhanced gene expression and biosynthesis of fumagillin. Viral RNA expression was enhanced during conidial maturation, conidial germination, and the mycelial stage. We presume that the RNA or translation products of the virus affected fungal phenotypes, including spore formation and toxin synthesis. To identify the mycovirus genes responsible for attenuation of fungal virulence, each viral ORF was ectopically expressed in the virus-free KU strain. We found that the expression of ORF2 and ORF5 reduced fungal virulence in the mouse model. In addition, ORF3 affected the stress tolerance of host A. fumigatus in culture. We hypothesize that the respective viral genes work cooperatively to suppress the pathogenicity of the fungal host.

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Full genome sequence of a new polymycovirus infecting Fusarium redolens

Cited by 19 publications

References 22 publications

Molecular Characterization of a Novel Polymycovirus From Penicillium janthinellum With a Focus on Its Genome-Associated PASrp

Molecular Characterization of a Novel Polymycovirus From Penicillium janthinellum With a Focus on Its Genome-Associated PASrp

Hadaka Virus 1: a Capsidless Eleven-Segmented Positive-Sense Single-Stranded RNA Virus from a Phytopathogenic Fungus, Fusarium oxysporum

Phenotypic and Molecular Biological Analysis of Polymycovirus AfuPmV-1M From Aspergillus fumigatus: Reduced Fungal Virulence in a Mouse Infection Model

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